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Biodiversita' Ed Evoluzione (Università Di Bologna) Alma Mater Studiorum – Università di Bologna in cotutela con Ghent University (Belgium) DOTTORATO DI RICERCA IN Biodiversita' ed Evoluzione (Università di Bologna) Ciclo 27 Settore Concorsuale di afferenza: 05/B1 Zoologia e Antropologia Settore Scientifico disciplinare: BIO/05 Zoologia PhD in Sciences, Marine Sciences (Ghent University) ASSESSMENT OF THE POPULATION STRUCTURE AND TEMPORAL CHANGES IN SPATIAL DYNAMICS AND GENETIC CHARACTERISTICS OF THE ATLANTIC BLUEFIN TUNA UNDER A FISHERY INDEPENDENT FRAMEWORK Presentata da: Gregory Neils Puncher Coordinatore Dottorato Relatore Prof. Barbara Mantovani Prof. Fausto Tinti Prof. Tom Moens Co-Relatore Dr. Haritz Arrizabalaga Esame finale anno 2015 “Assessment of the population structure and temporal changes in spatial dynamics and genetic characteristics of the Atlantic bluefin tuna under a fishery independent framework.” Doctoral Thesis Submitted to Alma Mater Studiorum - Università di Bologna & Universiteit Gent Academic Advisors Submitted by Fausto Tinti, PhD Gregory Neils Puncher, MSc Haritz Arrizabalaga, PhD UNIBO Matricola: 0900046704 Tom Moens, PhD UGent ID: 00914417 Departments of Scienze Biologiche, Geologiche ed Ambientali, Alma Mater Studiorum - Università di Bologna, Italia Marine Biology, Universiteit Gent, België Preface Due to rampant over-exploitation, the biomass of top predator species has declined by as much as 90% since the 1950s (Myers and Worm 2003). When these stocks have reached commercial exhaustion, fisheries have focused on the next lower trophic level, serially depleting marine resources in what has become known as “Fishing down food webs” (Pauly et al. 1998). Among commercially exploited fish, all three species of bluefin tuna (Pacific, Southern and Atlantic) have undergone some of the most significant declines in abundance and geographic range contractions (Worm and Tittensor 2011). As each of these species are large, long-lived, and have a high economic value, restricted spawning areas and short spawning periods, they are particularly susceptible to over-exploitation (Collette et al. 2011). Although the Atlantic bluefin tuna (BFT; Thunnus thynnus) has been targeted by fisheries in the Mediterranean Sea for thousands of years, it has only been in these last decades that the exploitation rate has reached far beyond sustainable levels; introducing a high risk of fisheries’ decline and stock collapse (MacKenzie et al. 2009). An understanding of the population dynamics, exploitation rates and the influence of environmental variables that affect large pelagic fish (e.g. tunas, billfishes and sharks) is crucial for stock management and conservation of entire marine ecosystems. In 2006, the International Commission for the Conservation of Atlantic Tunas (ICCAT) adopted a 15-year recovery plan for bluefin tuna in the eastern Atlantic and Mediterranean (EC N. 644/2007). In addition to the new restrictions placed on fisheries (restricted seasons, size limits, banning of search planes) a multidisciplinary monitoring programme was introduced in order to increase our understanding of the species' biological traits. Using an array of technologies (satellites tags, genetic markers and microchemistry of otoliths) researchers determined that the population structure of BFT is likely to be more complex than the current two population management model. A pattern indicative of genetic heterogeneity has been detected within the Mediterranean (Carlsson et al. 2004, 2007; Riccioni et al. 2010); rising suspicions that the basin may contain numerous distinct populations. Population structuring studies using of molecular tools should make use of samples with identified origins (ie. young tuna that haven't developed the capacity to travel great distances). Several genetic studies that analyzed adult specimens have been unable to detect significant differentiation of populations. Monitoring of early life history stages can also inform decision makers about the health of the species based upon recruitment and survival rates. PhD objectives In an effort to contribute to the conservation of the species and the development of a more informed stock assessment, this PhD project was developed to elucidate a more accurate understanding of BFT population structuring and spatial dynamics. The aims of the project were 1) to assess the accuracy of larval identification methods, 2) determine the genetic structure of modern BFT populations, 3) assess the self- recruitment rate in the Gulf of Mexico and Mediterranean spawning areas, 4) estimate the immigration rate of BFT to feeding aggregations from the various spawning areas, and 5) develop tools capable of investigating the temporal stability of population structuring in the Mediterranean Sea. Funding for the research contained in this thesis was by and large provided by ICCAT's Atlantic-wide Research Programme for Bluefin Tuna (GBYP) through the Biological and Genetic sampling and analyses consortium and the Data Recovery project conducted between 2012 and 2015. In order to establish a baseline of understanding concerning the basic biological traits of BFT, its morphological characteristics, geographic distribution and the fisheries that target them are detailed in Chapter 1. Current efforts to study BFT spatial dynamics and the tools used for estimating the remaining biomass are reviewed. Several inhibitory elements that challenge the development of effective conservation and management are also reviewed at length. Misidentification of larvae can lead to uncertainty about the spatial distribution of a species, confusion over life history traits and population dynamics, and potentially disguise the collapse or recovery of localized spawning areas. Chapter 2 details several weaknesses in modern morphology-based taxonomy including demographic decline of expert taxonomists, flawed identification keys, reluctance of the taxonomic community to embrace advances in digital communications and a general scarcity of modern user-friendly materials. Recent advances in molecular techniques useful for specimen identification and population studies are discussed at length. In this same vein, Chapter 3 contains a description of the molecular identification of larvae (n=188) collected from three spawning areas in the Mediterranean Sea by different institutions. Several techniques were used to analyze the genetic sequences and an extensive comparison of the results is presented. The results revealed important differences in the accuracy of the taxonomic identifications carried out by different ichthyoplanktologists following morphology-based methods. Molecular techniques used for wildlife conservation are evolving rapidly and their use by fisheries researchers is steadily on the increase. Using a Genotyping-by-Sequencing (a Next Generation Sequencing technique) approach a large consortium operating within the GBYP developed a panel of high performance SNPs capable of distinguishing populations of BFT. The process by which the 95 Single Nucleotide Polymorphisms (SNPs) were selected and technically validated is described in Chapter 4. This tool could be used to improve Atlantic BFT stock assessments and management as well as in seafood traceability studies and investigations. Chapter 5 details how the SNP panel was used to genotype 752 individuals captured between 2007-2013 from fourteen locations throughout the species' range, including several previously uncharacterized sites. Given the scale of sampling, this study is the most comprehensive assessment of modern bluefin tuna population structuring to date. These efforts were made with the aims to further validate the newly developed SNP panel as well as contribute to our understanding of the species' populations structuring. The results confirm much of what has already been learned from tagging and otolith studies with the exception of evidence suggestive of a small amount of mixing between eastern and western populations. Effective fishery management benefits from the existence of baseline information concerning population size and demographics before intense commercial exploitation. Given that BFT have been intensively targeted by fisheries for thousands of years, analysis of DNA extracted from historical samples recovered from archives, museums and archaeological excavations can help to reveal elements of the past necessary for establishing something of a pseudo-baseline (Nielsen et al. 1999). Chapter 6 provides a historical description of the relationship between humans and bluefin tuna, the state-of-the-art of historical DNA studies, and a description of new protocols developed for ancient DNA analysis. Using novel molecular techniques, DNA was extracted from bluefin tuna vertebrae excavated from late iron age and ancient roman settlements in coastal Iberia (Portual and Spain, 4th-2nd century BC; n=23) and Byzantine-era Constantinople (4th-15th century AD; n=6), as well as vertebrae from the Massimo Sella archive located at the University of Bologna (Ionian, Tyrrhenian and Adriatic Seas, early 20th century; n=150). In Chapter 7, I have described how a 96 SNP panel was developed to genotype historical and modern samples in order to elucidate changes in population structuring and allele frequencies of loci associated with selective traits. The panel is composed of 48 SNPs discovered during the GBS research that was described in the previous chapter (i.e. funded by ICCAT GBYP Phase 4). The remaining 48 SNPs were derived from transcriptomic work conducted in 2012 by the GenoDREAM laboratory (Pintus
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